An epigenetic mechanism mediates developmental nicotine effects on neuronal structure and behavior
Open accessAbstract
Developmental nicotine exposure causes persistent changes in cortical neuron morphology and in behavior. We used microarray screening to identify master transcriptional or epigenetic regulators mediating these effects of nicotine and discovered increases in Ash2l mRNA, encoding a component of a histone methyltransferase complex. We therefore examined genome-wide changes in trimethylation of histone H3 on Lys4 (H3K4me3), a mark induced by the Ash2l complex associated with increased gene transcription. A large proportion of regulated promoter sites were involved in synapse maintenance. We found that Mef2c interacts with Ash2l and mediates changes in H3K4me3. Knockdown of Ash2l or Mef2c abolished nicotine-mediated alterations of dendritic complexity in vitro and in vivo, and attenuated nicotine-dependent changes in passive avoidance behavior. In contrast, overexpression mimicked nicotine-mediated alterations of neuronal structure and passive avoidance behavior. These studies identify Ash2l as a target induced by nicotinic stimulation that couples developmental nicotine exposure to changes in brain epigenetic marks, neuronal structure and behavior.
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Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
Tissue-based map of the human proteome
Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., et al. (2015) · Science · doi:10.1126/science.1260419 · Cited by 15,286 · see citing works
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845 · see citing works
Epigenetics: A landscape takes shape
Goldberg, A. D., Allis, C. D., & Bernstein, E. (2007) · Cell · doi:10.1016/j.cell.2007.02.006 · Cited by 2,466 · see citing works
MEF2: a central regulator of diverse developmental programs
Potthoff, M. J., & Olson, E. N. (2007) · Development · doi:10.1242/dev.008367 · Cited by 834 · see citing works
Regulation of MLL1 H3K4 methyltransferase activity by its core components
Dou, Y., Milne, T. A., Ruthenburg, A. J., Lee, S., Lee, J. W., Verdine, G. L., Allis, C. D., & Roeder, R. G. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1128 · Cited by 764 · see citing works
Modes of neuronal migration in the developing cerebral cortex
Nadarajah, B., & Parnavelas, J. G. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn845 · Cited by 683 · see citing works
Gossett, L. A., Kelvin, D. J., Sternberg, E. A., & Olson, E. N. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.11.5022 · Cited by 600 · see citing works
Activity-Dependent Regulation of MEF2 Transcription Factors Suppresses Excitatory Synapse Number
Flavell, S. W., Cowan, C. W., Kim, T.-K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., & Greenberg, M. E. (2006) · Science · doi:10.1126/science.1122511 · Cited by 573 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
H3K4me3 Interactions with TAF3 Regulate Preinitiation Complex Assembly and Selective Gene Activation
Lauberth, S. M., Nakayama, T., Wu, X., Ferris, A. L., Tang, Z., Hughes, S. H., & Roeder, R. G. (2013) · Cell · doi:10.1016/j.cell.2013.01.052 · Cited by 473 · see citing works
A Calcium-Regulated MEF2 Sumoylation Switch Controls Postsynaptic Differentiation
Shalizi, A., Gaudilliere, B. L., Yuan, Z., Stegmüller, J., Shirogane, T., Ge, Q., Tan, Y. L., Schulman, B. A., Harper, J. W., & Bonni, A. (2006) · Science · doi:10.1126/science.1122513 · Cited by 456 · see citing works
Flavell, S. W., Kim, T.-K., Gray, J. M., Harmin, D. A., Hemberg, M., Hong, E. J., Markenscoff-Papadimitriou, E., Bear, D. M., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.11.029 · Cited by 440 · see citing works
Nicotine Decreases Food Intake Through Activation of POMC Neurons
Mineur, Y. S., Abizaid, A., Rao, Y., Salas, R., DiLeone, R. J., Gündisch, D., Diano, S., De Biasi, M., Horvath, T. L., Gao, X.-B., et al. (2011) · Science · doi:10.1126/science.1201889 · Cited by 439 · see citing works
Self-citationImprinting a determined state into the chromatin of Drosophila
Paro, R. (1990) · Trends in Genetics · doi:10.1016/0168-9525(90)90303-n · Cited by 380 · see citing works
Mineur, Y. S., Obayemi, A., Wigestrand, M. B., Fote, G. M., Calarco, C. A., Li, A. M., & Picciotto, M. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219731110 · Cited by 375 · see citing works
Self-citationLocal gene knockdown in the brain using viral-mediated RNA interference
Hommel, J. D., Sears, R. M., Georgescu, D., Simmons, D. L., & DiLeone, R. J. (2003) · Nature Medicine · doi:10.1038/nm964 · Cited by 334 · see citing works
Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes
Steward, M., Lee, J., O’Donovan, A., Wyatt, M., Bernstein, B., & Shilatifard, A. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1131 · Cited by 325 · see citing works
Barbosa, A. C., Kim, M.-S., Ertunc, M., Adachi, M., Nelson, E. D., McAnally, J., Richardson, J. A., Kavalali, E. T., Monteggia, L. M., Bassel-Duby, R., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802679105 · Cited by 303 · see citing works
Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation
Lyons, G., Micales, B. K., Schwarz, J. J., Martin, J., & Olson, E. N. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05727.1995 · Cited by 271 · see citing works
Li, H., Radford, J. C., Ragusa, M. J., Shea, K. L., McKercher, S. R., Zaremba, J. D., Soussou, W., Nie, Z., Kang, Y., Nakanishi, N., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802876105 · Cited by 254 · see citing works
Histone arginine methylation and its dynamic regulation
Wysocka, J. (2006) · Frontiers in bioscience · doi:10.2741/1802 · Cited by 233 · see citing works
Rampalli, S., Li, L., Mak, E., Ge, K., Brand, M., Tapscott, S. J., & Dilworth, F. J. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1316 · Cited by 213 · see citing works
Mazo, A., Huang, D. H., Mozer, B. A., & Dawid, I. B. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.6.2112 · Cited by 194 · see citing works
Zweier, M., Gregor, A., Zweier, C., Engels, H., Sticht, H., Wohlleber, E., Bijlsma, E. K., Holder, S., Zenker, M., Rossier, E., et al. (2010) · Human Mutation · doi:10.1002/humu.21253 · Cited by 180 · see citing works
Gossett, L. A., Kelvin, D. J., Sternberg, E. A., et al. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.11.5022-5033.1989 · Cited by 159 · see citing works
Pauly, J. R., Sparks, J. A., Hauser, K. F., & Pauly, T. H. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.009 · Cited by 113 · see citing works
Heath, C. J., & Picciotto, M. R. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.020 · Cited by 99 · see citing works
Self-citationThe effects of prenatal nicotine on radial-arm maze performance in rats
Sorenson, C. A., Raskin, L. A., & Suh, Y. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90117-k · Cited by 97 · cited 4× · see citing works
“Bottom, nicotine (Nic) treatment from E14 through P21 induced hypersensitive passive avoidance behavior that was attenuated by knockdown of Ash2l or Mef2c (F(5,135) = 2.”
InfluentialAlterations of cortical pyramidal neurons in mice lacking high-affinity nicotinic receptors
Ballesteros-Yáñez, I., Benavides-Piccione, R., Bourgeois, J.-P., Changeux, J.-P., & DeFelipe, J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006269107 · Cited by 96 · see citing works
Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats
Sobrian, S. K., Marr, L., & Ressman, K. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00042-3 · Cited by 92 · see citing works
Development of the Human Fetal Auditory Cortex: Growth of Afferent Fibres
Krmpotić‐Nemanić, J., Kostović, I., Kelović, Z., Nemanić, Đ., & Mrzljak, L. (1983) · Cells Tissues Organs · doi:10.1159/000145727 · Cited by 89 · see citing works
King, S. L., Marks, M. J., Grady, S. R., Caldarone, B. J., Koren, A. O., Mukhin, A. G., Collins, A. C., & Picciotto, M. R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03837.2003 · Cited by 82 · see citing works
Self-citationWan, M., Liang, J., Xiong, Y., Shi, F.-T., Zhang, Y., Lu, W., He, Q., Yang, D., Chen, R., Liu, D., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.424515 · Cited by 76 · see citing works
Adamson, A. L., & Shearn, A. (1996) · Genetics · doi:10.1093/genetics/144.2.621 · Cited by 72 · see citing works
Induction of Dendritic Spines by 2-Containing Nicotinic Receptors
Lozada, A. F., Wang, X., Gounko, N. V., Massey, K. A., Duan, J., Liu, Z., & Berg, D. K. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6247-11.2012 · Cited by 65 · see citing works
Heath, C. J., King, S. L., Gotti, C., Marks, M. J., & Picciotto, M. R. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.130 · Cited by 59 · see citing works
Self-citationPrenatal nicotine exposure alters neuroanatomical organization of the developing brain
Muhammad, A., Mychasiuk, R., Nakahashi, A., Hossain, S. R., Gibb, R. L., & Kolb, B. E. (2012) · Synapse · doi:10.1002/syn.21589 · Cited by 57 · see citing works
Maćkowiak, M., Bator, E., Latusz, J., Mordalska, P., & Wędzony, K. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.05.013 · Cited by 51 · see citing works
Cho, E., Zaremba, J. D., McKercher, S. R., Talantova, M. V., Tu, S., Masliah, E., Chan, S. F., Nakanishi, N., Terskikh, A. V., & Lipton, S. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024027 · Cited by 49 · see citing works
Mychasiuk, R., Muhammad, A., Gibb, R. L., & Kolb, B. E. (2013) · Brain Research · doi:10.1016/j.brainres.2012.12.021 · Cited by 49 · see citing works
Tan, C. C., Sindhu, K. V., Li, S., Nishio, H., Stoller, J. Z., Oishi, K., Puttreddy, S., Lee, T. J., Epstein, J. A., Walsh, M. J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711896105 · Cited by 42 · see citing works
Development of Acetylcholinesterase (Ache) Staining in Human Fetal Auditory Cortex
Krmpotić‐Nemanić, J., Kostović, I., Kelović, Z., & Nemanić, Đ. (1980) · Acta Oto-Laryngologica · doi:10.3109/00016488009127153 · Cited by 41 · see citing works
Heath, C. J., Horst, N. K., & Picciotto, M. R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.021 · Cited by 38 · see citing works
Self-citationJacobsen, L. K., Picciotto, M. R., Heath, C. J., Mencl, W. E., & Gelernter, J. E. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.024 · Cited by 38 · see citing works
Self-citationIkegawa, S., Isomura, M., Koshizuka, Y., & Nakamura, Y. (1999) · Cytogenetic and Genome Research · doi:10.1159/000015248 · Cited by 32 · see citing works
Cheng, M. K., & Shearn, A. (2004) · Genetics · doi:10.1534/genetics.103.018721 · Cited by 32 · see citing works
Isolation, Culture, and Differentiation of Progenitor Cells from the Central Nervous SystemPreprint
Hutton, S. R., & Pevny, L. (2008) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5077 · Cited by 29 · see citing works
Neuroanatomical changes in a mouse model of early life neglect
Duque, A., Coman, D., Carlyle, B. C., Bordner, K. A., George, E. D., Papademetris, X., Hyder, F., & Simen, A. A. (2012) · Brain Structure and Function · doi:10.1007/s00429-011-0350-9 · Cited by 28 · see citing works
Self-citationSakai, Y., Ohkubo, K., Matsushita, Y., Akamine, S., Ishizaki, Y., Torisu, H., Ihara, K., Sanefuji, M., Kim, M., Lee, K., et al. (2013) · European Journal of Medical Genetics · doi:10.1016/j.ejmg.2013.06.009 · Cited by 8 · see citing works
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Ballinger, E. C., Ananth, M. R., Talmage, D. A., & Role, L. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.006 · Cited by 735 · see citing works
Principles of plasticity in the developing brain
Kolb, B. E., Harker, A., & Gibb, R. L. (2017) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13546 · Cited by 197 · see citing works
Sarker, G., Sun, W., Rosenkranz, D., Pelczar, P., Opitz, L., Efthymiou, V., Wolfrum, C., & Peleg‐Raibstein, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820810116 · Cited by 160 · see citing works
Nicotine on the developing brain.
Castro, E. M., Lotfipour, S., & Leslie, F. M. (2023) · Pharmacological research · doi:10.1016/j.phrs.2023.106716 · Cited by 140 · see citing works
Cecil, C. A. M., Walton, E., Smith, R. G., Viding, E., McCrory, E. J., Relton, C. L., Suderman, M., Pingault, J.-B., McArdle, W., Gaunt, T. R., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.247 · Cited by 101 · see citing works
Emerging roles for MEF2 in brain development and mental disorders
Assali, A., Harrington, A. J., & Cowan, C. W. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.04.008 · Cited by 92 · see citing works
Can epigenetics translate environmental cues into phenotypes?
Norouzitallab, P., Baruah, K., Vanrompay, D. C. G., & Bossier, P. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.08.063 · Cited by 79 · see citing works
Jung, Y., Lee, A. M., McKee, S. A., & Picciotto, M. R. (2017) · Scientific Reports · doi:10.1038/s41598-017-04413-1 · Cited by 77 · see citing works
Self-citationDougnon, G., & Matsui, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147550 · Cited by 71 · see citing works
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Koukouli, F., & Changeux, J. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.06.001 · Cited by 61 · see citing works
Buck, J. M., Sanders, K. N., Wageman, C., Knopik, V., Stitzel, J., & O’Neill, H. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.02.006 · Cited by 49 · see citing works
The complex activities of the SET1/MLL complex core subunits in development and disease
Jiang, H. (2020) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2020.194560 · Cited by 58 · see citing works
Progress on the Roles of MEF2C in Neuropsychiatric Diseases
Zhang, Z., & Zhao, Y. (2022) · Molecular Brain · doi:10.1186/s13041-021-00892-6 · Cited by 56 · see citing works
Chang, L., Oishi, K., Skranes, J. S., Buchthal, S. D., Cunningham, E. P., Yamakawa, R., Hayama, S., Jiang, C. S., Alicata, D., Hernandez, A., et al. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.2794 · Cited by 55 · see citing works
Epigenetic and long-term effects of nicotine on biology, behavior, and health
Gould, T. J. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106741 · Cited by 58 · see citing works
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Becchetti, A., Grandi, L. C., Cerina, M., & Amadeo, A. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106698 · Cited by 53 · see citing works
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Lisek, M., Przybyszewski, O., Żylińska, L., Guo, F., & Boczek, T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043120 · Cited by 45 · see citing works
Goldberg, L. R., Zeid, D., Kutlu, M. G., Cole, R. D., Lallai, V., Sebastian, A., Albert, I. U., Fowler, C. D., Parikh, V., & Gould, T. J. (2019) · Addiction Biology · doi:10.1111/adb.12859 · Cited by 38 · see citing works
Neuroepigenetics and addictive behaviors: Where do we stand?
Nogueira, D. D. S., Mérienne, K., & Befort, K. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.018 · Cited by 38 · see citing works
Li, L., Ruan, X., Wen, C., Chen, P., Liu, W., Zhu, L., Xiang, P., Zhang, X., Wei, Q., Hou, L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.055 · Cited by 31 · see citing works
Agrawal, P., Chung, P., Heberlein, U., & Kent, C. F. (2019) · BMC Biology · doi:10.1186/s12915-019-0646-4 · Cited by 29 · see citing works
Tobacco and alcohol use during adolescence: Interactive mechanisms in animal models
Abreu‐Villaça, Y., Manhães, A. C., Krahe, T. E., Filgueiras, C. C., & Ribeiro‐Carvalho, A. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.06.113 · Cited by 28 · see citing works
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Huang, Z., Wu, D., Qu, X., Li, M., Zou, J., & Tan, S. (2020) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0044 · Cited by 27 · see citing works
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Baratta, A. M., Rathod, R. S., Plasil, S. L., Seth, A., & Homanics, G. E. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.08.003 · Cited by 28 · see citing works
Zeng, K., Wu, Y. M., Wang, C., Wang, S., Sun, H., Zou, R., Sun, G., Song, H., Liu, W., Sun, N., et al. (2020) · Cancer Science · doi:10.1111/cas.14413 · Cited by 26 · see citing works
Reynolds, L. M., Faure, P., & Barik, J. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03110-0 · Cited by 26 · see citing works
“Exposure to nicotine in adolescence may also produce enduring epigenetic changes, like those seen after pre-natal and juvenile exposure to nicotine [159].”
Micalizzi, L., & Knopik, V. S. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001687 · Cited by 25 · see citing works
Su, W., Lin, Y., Wong, S., Chen, J. Y., Lee, J., & Buu, A. (2021) · Journal of Exposure Science & Environmental Epidemiology · doi:10.1038/s41370-021-00362-0 · Cited by 24 · see citing works
Epigenetic mechanisms of nicotine dependence
Muenstermann, C., & Clemens, K. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105505 · Cited by 24 · see citing works
Lee, A. M., Mansuri, M. S., Wilson, R. S., Lam, T. T., Nairn, A. C., & Picciotto, M. R. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.657064 · Cited by 23 · see citing works
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Fowler, C. D., Gipson, C. D., Kleykamp, B. A., Rupprecht, L. E., Harrell, P. T., Rees, V. W., Gould, T. J., Oliver, J. A., Bağdaş, D., Damaj, M. I., et al. (2017) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntx175 · Cited by 23 · see citing works
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Polli, F. S., & Kohlmeier, K. A. (2019) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntz196 · Cited by 23 · see citing works
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Gitik, M., Holliday, E. D., Leung, M., Yuan, Q., Logue, S. F., Tikkanen, R., Goldman, D., & Gould, T. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.08.009 · Cited by 21 · see citing works
Self-citationMcCarthy, D. M., Lowe, S. E., Morgan, T. J., Cannon, E. N., Biederman, J., Spencer, T. J., & Bhide, P. G. (2020) · Scientific Reports · doi:10.1038/s41598-020-68883-6 · Cited by 22 · see citing works
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Lo, J. O.-T., Hedges, J. C., Chou, W. H., Tager, K. R., Bachli, I., Hagen, O. L., Murphy, S. K., Hanna, C. B., & Easley, C. A. (2024) · Nature Reviews Urology · doi:10.1038/s41585-024-00868-w · Cited by 22 · see citing works
Khalifeh, M., Hobeika, R., Hayek, L. E., Saad, J., Eid, F., Khoury, R. E., Ghayad, L. M., Jabre, V., Nasrallah, P., Barmo, N., et al. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112499 · Cited by 18 · see citing works
Calarco, C. A., Lee, S., & Picciotto, M. R. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.06.012 · Cited by 17 · see citing works
Self-citationMahmood, H. M., Aldhalaan, H., Alshammari, T. K., Alqasem, M., Alshammari, M. A., Albekairi, N. A., & AlSharari, S. D. (2020) · Autism Research · doi:10.1002/aur.2342 · Cited by 17 · see citing works
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Alzu’bi, A., Middleham, W., Shoaib, M. C., & Clowry, G. J. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00072 · Cited by 13 · see citing works
Lee, H.-Y., Jeon, Y., Kim, Y. K., Jang, J. Y., Cho, Y. S., Bhak, J., & Cho, K. (2021) · Scientific Reports · doi:10.1038/s41598-021-91811-1 · Cited by 13 · see citing works
Fan, L., Chen, H., Liu, Y. U., Hou, H., & Hu, Q. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173510 · Cited by 13 · see citing works
Miller, M. B., Wilson, R. S., Lam, T. T., Nairn, A. C., & Picciotto, M. R. (2018) · Proteomes · doi:10.3390/proteomes6040042 · Cited by 13 · see citing works
Self-citationWang, Y. J., Zhang, X., Lam, C. K., Guo, H., Wang, C., Zhang, S., Wu, J. C., Snyder, M. P., & Li, J. (2022) · Cell Systems · doi:10.1016/j.cels.2022.09.001 · Cited by 11 · see citing works
Effects of prenatal exposure to THC on hippocampal neural development in offspring
Peng, H., Li, H., Wei, Y., Zhang, R., Chang, X., Meng, L., Wang, K., He, Q., & Duan, T. (2022) · Toxicology Letters · doi:10.1016/j.toxlet.2022.12.007 · Cited by 12 · see citing works
Buck, J. M., Yu, L., Knopik, V. S., & Stitzel, J. A. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab138 · Cited by 11 · see citing works
Epigenetic Mechanisms Mediate Nicotine-Induced Reward and Behaviour in Zebrafish
Faillace, M. P., & Bernabeu, R. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210716112351 · Cited by 11 · see citing works
Hayase, T. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000326 · Cited by 11 · see citing works
Lee, B., Park, S. M., Jeong, S., Kim, K., & Jeung, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147742 · Cited by 10 · see citing works
Collo, G., Cavalleri, L., Zoli, M., Maskos, U., Ratti, E., & Pich, E. M. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00572 · Cited by 10 · see citing works
The influence of adolescent nicotine exposure on ethanol intake and brain gene expression
Silva, C. P., Horton, W. J., Caruso, M. J., Sebastian, A., Klein, L. C., Albert, I. U., & Kamens, H. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198935 · Cited by 10 · see citing works
An Update on the Role of Common Genetic Variation Underlying Substance Use Disorders
Johnson, E. C., Chang, Y., & Arpana Agrawal, A. (2020) · Current Genetic Medicine Reports · doi:10.1007/s40142-020-00184-w · Cited by 9 · see citing works
Keifer, J. (2017) · Genes · doi:10.3390/genes8020069 · Cited by 10 · see citing works
White matter abnormalities in the Hdc knockout mouse, a model of tic and OCD pathophysiology
Jindachomthong, K., Yang, C., Huang, Y., Coman, D., Rapanelli, M., Hyder, F., Dougherty, J. D., Frick, L. R., & Pittenger, C. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1037481 · Cited by 9 · see citing works
Self-citationEstimation of Health Risks Caused by Metals Contained in E-Cigarette Aerosol through Passive Vaping
Su, W., Lee, J., Zhang, K., Wong, S., & Buu, A. (2023) · Toxics · doi:10.3390/toxics11080684 · Cited by 9 · see citing works
Grillberger, K., Cöllen, E., Trivisani, C. I., Blum, J. H., Leist, M., & Ecker, G. F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713170 · Cited by 12 · see citing works
Puberty exposure to cigarette smoke extract impairs adult spermatogenesis in the mouse
Zhao, G., Mo, J., Zheng, T., Li, Y., Wu, X., Huang, J. R., Liu, G., Huang, Z., & Yu, B. (2018) · Reproductive Toxicology · doi:10.1016/j.reprotox.2018.10.012 · Cited by 9 · see citing works
The function of Mef2c toward the development of excitatory and inhibitory cortical neurons
Ward, C., Sjulson, L., & Batista‐Brito, R. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1465821 · Cited by 8 · see citing works
Lin, L., Ou, X.-X., Zhan, X., Wang, X., Cai, L., Li, X., Jin, J., & Dong, G. (2022) · World Journal of Pediatrics · doi:10.1007/s12519-022-00644-z · Cited by 8 · see citing works
Rodríguez-Vega, A., Dutra-Tavares, A. C., de Souza, T. P., Semeão, K. A., Filgueiras, C. C., Ribeiro‐Carvalho, A., Manhães, A. C., & Abreu‐Villaça, Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914634 · Cited by 7 · see citing works
Enduring effects of perinatal nicotine exposure on murine sleep in adulthood.
Borniger, J. C., Don, R. F., Zhang, N., Boyd, R., & Nelson, R. (2017) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00156.2017 · Cited by 6 · see citing works
Meneghini, S., Modena, D., Colombo, G., Coatti, A., Milani, N., Madaschi, L., Amadeo, A., & Becchetti, A. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102279 · Cited by 5 · see citing works
Dissecting the epigenomic differences between smoking and nicotine dependence in a veteran cohort
Nagamatsu, S. T., Pietrzak, R. H., Xu, K., Krystal, J. H., Gelernter, J. E., & Montalvo‐Ortiz, J. L. (2022) · Addiction Biology · doi:10.1111/adb.13259 · Cited by 5 · see citing works
Effect of Grandmaternal Smoking on Body Size and Proportions at Birth
Rumrich, I. K., Hänninen, O., Viluksela, M., & Vähäkangas, K. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18094985 · Cited by 5 · see citing works
Szapuova, Z. J., Argalášová, Ľ., Vondrová, D., Janšáková, K., Belica, I., Kopčíková, M., Babinská, K., & Ostatníková, D. (2022) · Toxics · doi:10.3390/toxics10040189 · Cited by 4 · see citing works
Noble, A. J., Pearson, J. F., Noble, A. D. L., Boden, J. M., Horwood, L. J., Kennedy, M. A., & Osborne, A. J. (2022) · Reproduction Fertility and Development · doi:10.1071/rd21108 · Cited by 4 · see citing works
Lee, A. M., & Picciotto, M. R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.04.007 · Cited by 4 · see citing works
Self-citationNoble, A. J., Pearson, J. F., Noble, A. D., Boden, J. M., Horwood, L. J., Kennedy, M. A., & Osborne, A. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.02.183285 · Cited by 4 · see citing works
Uygun, S. D., Kose, T. B., Bahadır‐Varol, A., Uzay, B., & Eren‐Koçak, E. (2025) · Acta Neuropsychiatrica · doi:10.1017/neu.2025.2 · Cited by 3 · see citing works
Chen, Z., Song, L., Chen, W., & Wang, C. (2025) · Communications Biology · doi:10.1038/s42003-025-08683-8 · Cited by 4 · see citing works
Histone Methyltransferase G9a Plays an Essential Role on Nicotine Preference in Zebrafish
Faillace, M. P., Ortiz, J., Rocco, L., & Bernabeu, R. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-03961-8 · Cited by 3 · see citing works
Su, H., Nakauchi, S., & Sumikawa, K. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107674 · Cited by 3 · see citing works
Zhao, Y., Li, B. J., Cao, H., Wang, F., Mu, M., Jin, H., Liu, J., Fan, Z., & Tao, X. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.116079 · Cited by 3 · see citing works
Epigenetics, behavior and early nicotine
Maldonado, R. J., & Martín, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4330 · Cited by 3 · see citing works
Destined to travel? Unlocking the genetic roots of tourist behaviour
Hu, F., Wen, J., Ying, T., Goh, B. K., & Wang, W. (2026) · Tourism Recreation Research · doi:10.1080/02508281.2026.2637466 · Cited by 1 · see citing works
Nusir, A., Anthony, S. M., Zhou, W., & Kabbani, N. (2026) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5c01027 · Cited by 1 · see citing works
Mechanisms underlying the enduring addiction vulnerability conferred by nicotine in adolescence
Reynolds, L. M. (2026) · Addiction Neuroscience · doi:10.1016/j.addicn.2026.100272 · Cited by 1 · see citing works
Early life substance abuse and epigenetic programming
Leyrer‐Jackson, J. M., Hood, L. E., & Olive, M. F. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821785-6.00008-6 · Cited by 1 · see citing works
Shehata, M. A., El-Din, E. M. S., Youssef, M. M., Shady, M. M. A., El-Alameey, I. R., Ashaat, E. A., Gouda, A. S., & Nazim, W. S. (2021) · Open Access Macedonian Journal of Medical Sciences · doi:10.3889/oamjms.2021.7635 · Cited by 1 · see citing works
Burke, A. P. (2016) · TSpace (University of Toronto) · Cited by 1 · see citing works
Fetal Nicotine Exposure Has Enduring Effects on Brain Development
Dubovsky, S. L. (2016) · Journal watch · doi:10.1056/nejm-jw.na41761
Zhang, W., Deng, X., Liu, H., Ke, J., Xiang, M., Ma, Y., Zhang, L., Yang, M. J., Liu, Y., & Huang, F. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.837123
Wang, Y. J., Zhang, X., Lam, C. K., Guo, H., Wang, C., Zhang, S., Wu, J. C., Snyder, M. P., & Li, J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.23.496464
Epigenetic-focused CRISPR/Cas9 screen identifies ASH2L as a regulator of glioblastoma cell survivalPreprint
Ozyerli‐Goknar, E., Kala, E. Y., Aksu, A. C., Bulut, İ., Cingöz, A., Nizamuddin, S., Biniossek, M. L., Seker-Polat, F., Morova, T., Aztekin, C., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.17.504245
Developmental, epigenetic, and possible transgenerational effects of smoking and vaping
Boyd, R. T. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-819958-9.00011-6
Roles for the MEF2 Transcription Factors in Synapse and Circuit Development and Plasticity
Zhang, Z., & Huber, K. M. (2024) · Springer eBooks · doi:10.1007/978-3-031-68550-7_11
Li, X., Ma, J.-J., Meng, L., Han, Z., Li, Q.-L., Yang, X., Xie, L., & Jiang, L. (2025) · Seizure · doi:10.1016/j.seizure.2025.12.003
Buck, J. M., Melnick, M., & Stitzel, J. A. (2026) · Genes · doi:10.3390/genes17020128
Nogueira, D. D. S. (2019) · theses.fr (ABES) · doi:10.70675/d429d5dbz5001z4e60z9622z4f636e667f17
Delgado, M., Roja, A., Pareek, O., Penman, S. L., Smith, D., & Thanos, P. K. (2026) · Immunological Investigations · doi:10.1080/08820139.2026.2752371
- Authors
- Jung, Y., Hsieh, L. S., Lee, A. M., Zhou, Z., Coman, D., Heath, C. J., Hyder, F., Mineur, Y. S., Yuan, Q., Goldman, D., Bordey, A., & Picciotto, M. R.
- Affiliations
- Yale University (US)
- National Institute on Alcohol Abuse and Alcoholism (US)
- The Open University (GB)
- Corresponding author
- Picciotto, Marina R
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2016-05-30
- Volume
- 19
- Issue
- 7
- Pages
- 905-914
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4925298
- OpenAlex
- W2417118842
- Cited by
- 90
- References
- 50
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 5 · 2023: 10 · 2022: 15 · 2021: 9 · 2020: 11 · 2019: 9 · 2018: 7 · 2017: 9 · 2016: 6
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Open Research Online - ORO (The Open University) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (UL1TR001863)
- National Institute of Mental Health (R01MH067528)
- National Institute on Drug Abuse (R01DA014241, R29DA010455, R01DA010455, R37DA014241)
- National Institute of General Medical Sciences (T32GM007205)
- National Institute of Neurological Disorders and Stroke (R01NS086329, P30NS052519)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- epigenetics, ASH2L, MEF2C, histone methyltransferase complex, H3K4 trimethylation, dendritic complexity, cortical neurons, synapse maintenance, neuronal morphology
- MeSH terms
- Animals, DNA-Binding Proteins, Histones, Methylation, Mice, Inbred C57BL, Nicotine, Nuclear Proteins, Promoter Regions, Genetic, Histone-Lysine N-Methyltransferase, Transcription Factors, Epigenesis, Genetic
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